University of Groningen The impact of the invisible Buunk, Anne Marie

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The impact of the invisible

Buunk, Anne Marie

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2019

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Buunk, A. M. (2019). The impact of the invisible: Cognitive deficits, behavioral changes, and fatigue after

subarachnoid hemorrhage. Rijksuniversiteit Groningen.

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8 Introducing subarachnoid hemorrhage

A subarachnoid hemorrhage (SAH) is a severe bleeding in the subarachnoid

space, between the pia mater and the arachnoid membrane. In the majority of

cases, SAH is characterized by the rupture of an intracranial aneurysm, defined

as aneurysmal SAH (aSAH). In 15% of the cases of SAH, no structural cause

for the hemorrhage can be detected, typed as angiographically negative SAH

(anSAH). SAH accounts for only 3-5% of all strokes, but is the type of stroke with

the highest morbidity and mortality rates (Feigin, Lawes, Bennett, Barker-Collo,

& Parag, 2009). The incidence of SAH in the Netherlands is between 5 and 7

cases per 100,000 per year (Risselada et al., 2011). A SAH still carries a case

fatality of approximately 35%, despite the fact that this is reduced during the

past thirty years, mostly because new diagnostic techniques and therapeutic

interventions have emerged (Rinkel & Algra, 2011). Generally, aSAH is treated

by either endovascular treatment (coiling and/or stenting) or microsurgical

occlusion (clipping or wrapping) of the aneurysm.

A sudden severe headache is the most distinctive symptom of SAH.

Other symptoms are neck stiffness, nausea, photophobia, focal neurological

deficits or unconsciousness. Main complications are acute hydrocephalus,

rebleeding, and vasospasm, with possible delayed cerebral ischemia (van Gijn,

Kerr, & Rinkel, 2007). Acute hydrocephalus is generally treated with an external

ventricular drain or external lumbar drain. Hydrocephalus that persists beyond

the acute stage, i.e. chronic hydrocephalus, requires cerebrospinal fluid (CSF)

shunting.

Emotional, cognitive, and behavioral consequences

SAH has a great impact both on the patient and relatives. Cognitive impairment

may occur in up to 83% of cases, with main cognitive domains being affected:

memory, attention, and language (Al-Khindi, Macdonald, & Schweizer, 2010;

Kapadia, Schweizer, Spears, Cusimano, & Macdonald, 2014). However, most

of the studies on post-SAH cognitive functioning have focused on patients

after aneurysmal SAH, not after angiographically negative SAH. In general, it is

suggested that cognitive deficits can remain over years. Cognitive impairment

has been associated with clinical features such as hydrocephalus and delayed

cerebral ischemia (Ogden, Mee, & Henning, 1993) and demographic variables

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9 such as high age and low education (Kreiter et al., 2002).

Next to objective cognitive deficits as assessed with neuropsychological

tests, SAH patients report a wide range of cognitive complaints, such as

forgetfulness or planning problems. Furthermore, behavioral problems are often

mentioned after SAH, for example apathy (Marin, Biedrzycki, & Firinciogullari,

1991) and inadequate social behavior (Ogden, Utley, & Mee, 1997; Storey,

1970). These behavioral problems are usually measured with self-report

questionnaires, but could possibly also be examined using neuropsychological

assessment.

Lastly, mood disorders, sleep disturbances and fatigue are major

post-SAH consequences (Kutlubaev, Barugh, & Mead, 2012; Rinkel & Algra, 2011;

Schuiling, Rinkel, Walchenbach, & de Weerd, 2005). Reported frequencies of

fatigue are high (up to 90%) and the numbers vary depending on the instrument

used and timing of testing. Depression and anxiety are common after SAH,

with prevalence rates up to 54% (Al-Khindi, Macdonald, & Schweizer, 2010;

Boerboom, Heijenbrok-Kal, Khajeh, van Kooten, & Ribbers, 2016; Caeiro, Santos,

Ferro, & Figueira, 2011; Hedlund, Zetterling, Ronne-Engstrom, Carlsson, &

Ekselius, 2011), and presence of symptoms even in the chronic stage post-SAH

(Ackermark et al., 2017; von Vogelsang, Forsberg, Svensson, & Wengstrom,

2015). Additionally, post-traumatic stress disorder (PTSD) has been described

in SAH patients, with rates varying between 18% and 34% (Huenges Wajer

et al., 2018; Hutter & Andermahr, 2014; Hutter,

Kreitschmann-Andermahr, & Gilsbach, 2001; Noble et al., 2011; Visser-Meily et al., 2013).

Functional outcome

As SAH usually occurs at a relatively young age (mean age of 55 years),

post-SAH consequences may influence daily functioning for many years (de Rooij,

Linn, van der Plas, Algra, & Rinkel, 2007). Although recovery to functional

independence is common, many patients still experience a reduced Quality of

Life (QoL) (Hackett & Anderson, 2000; Hop, Rinkel, Algra, & van Gijn, 2001).

Furthermore, return to work is seriously affected after SAH; up to two-thirds of all

patients are unable to return to their pre-SAH employment (Passier, Visser-Meily,

Rinkel, Lindeman, & Post, 2011; Powell, Kitchen, Heslin, & Greenwood, 2004).

Also, changes in social participation and leisure activities have been reported

(Carter, Buckley, Ferraro, Rordorf, & Ogilvy, 2000; Johansson, Hogberg, &

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10 Bernspang, 2007). Different factors have been related to problems in everyday

life functioning, such as cognitive complaints, mood disorders, and behavioral

disturbances (Carter et al., 2000; Morris, Wilson, & Dunn, 2004; Ogden et al.,

1997; Vilkki, Juvela, Malmivaara, Siironen, & Hernesniemi, 2012).

Aneurysmal SAH versus angiographically negative

SAH

Traditionally, anSAH has been regarded as a benign entity, considering the good

overall neurological outcomes and low risk of rebleeding (Rinkel et al., 1991;

Ruelle, Lasio, Boccardo, Gottlieb, & Severi, 1985). More recently, persistent

complaints of fatigue, mood disorders, and behavioral problems have been

found after anSAH (Alfieri et al., 2008; Canhao, Ferro, Pinto, Melo, & Campos,

1995; Marquardt, Niebauer, Schick, & Lorenz, 2000). Studies on the cognitive

consequences of anSAH show conflicting results; some authors reported

cognitive functions in the normal range (Germano et al., 1998; Krajewski et al.,

2014), others found evidence for cognitive impairment post-anSAH (Boerboom,

Heijenbrok-Kal, Khajeh, van Kooten, & Ribbers, 2014; Hutter, Gilsbach, &

Kreitschmann, 1994; Sonesson, Saveland, Ljunggren, & Brandt, 1989). Also,

two studies revealed problems in the resumption of daily activities after anSAH,

comparable to those after aSAH (Alfieri, Gazzeri, Pircher, Unterhuber, &

Schwarz, 2011; Canhao et al., 1995).

Higher-order prefrontal cognitive functions

Although behavioral disturbances, such as apathy and inadequate social

behavior, are frequently reported after SAH, the underlying mechanism is

unclear. Over thirty years ago, Brooks (1984) already recognized the need to

investigate behavioral consequences of brain injury. He argued that especially

behavioral problems negatively affect everyday life functioning and cause stress

for families and caregivers. Over the course of years, researchers have shown

an increased interest in the assessment and treatment of these behavioral

disturbances. Specifically, recent studies have focused on the underlying

neuropsychological mechanisms of these problems and concentrated on the

objective neuropsychological assessment of social behavioral changes. This

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11 has led to the hypothesis that impairments in so called higher-order prefrontal

cognitive functions, executive functions and social cognition, may underlie

changes in behavior and social competence.

Executive functions comprise those mental capacities needed to

initiate, monitor, and regulate complex, goal-directed behavior (Lezak, 1995).

These capacities allow us to adapt to new, unstructured situations. Symptoms

of executive dysfunction are for instance impulsivity, impaired abstract thinking,

poor decision making, and perseveration (Burgess & Simons, 2005). Social

cognition is defined as the ability to understand others’ behavior and react

adequately in social situations (Adolphs, 2001; Lieberman, 2007). Different

aspects can be distinguished, such as the recognition of facial emotional

expressions and understanding someone else’s behavior and intentions. A

distinction is often drawn between ‘hot’ social cognition, that is the ability to

understand others’ emotional states and to show empathy, and ‘cold’ social

cognition, that is thinking about something from another person’s point of view

(Blair, 2003). An important aspect of cold social cognition is Theory of Mind

(ToM): the ability to understand behavior of others, based on their feelings,

beliefs, intentions, and experiences. Deficits in social cognition can manifest

themselves in several ways; symptoms are for example inappropriate behavior,

an inability to show empathy or diminished interest in others.

The prefrontal cortex, as a part of cortical-subcortical circuits, plays

a key role in both executive functions and social cognition, hence the name

‘higher-order prefrontal cognitive functions’. More specifically, the dorsolateral

prefrontal cortex is important for executive functions and the orbitofrontal and

ventromedial prefrontal cortices are mainly involved in social cognition (Lichter

& Cummings, 2001). However, these prefrontal areas are largely overlapping

regions, and executive functions and social cognition are not solely located in the

frontal areas of the brain (Tekin & Cummings, 2002). Therefore, it is interesting to

investigate the relationship between higher-order cognitive functions and focal

(frontal) as well as diffuse brain damage.

General aim and outline of this dissertation

The main objective of this thesis is to investigate several neuropsychological

consequences of subarachnoid hemorrhage, namely cognitive impairments,

behavioral problems, and fatigue, and to define their mutual relationship with

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12 long-term outcome. Specifically, this project set out to examine impairments

in higher-order prefrontal cognitive functions, social cognition and executive

functions, after SAH. A better characterization of post-SAH consequences

and their predictive value leads to a better understanding of the nature of

disturbances and consequently, can lead to better treatment methods.

First, a general introduction to the subject is given (Chapter 1). In

chapter 2 , a study on long-term resumption of leisure and social activities is

presented, focusing on the influence of executive complaints and lesion location.

Chapter 3 presents a study on two major characteristics of fatigue (mental and

physical fatigue) and their relationship with long-term functional outcome after

SAH. Chapter 4 comprises a description of the cognitive consequences of

SAH and comparisons between aSAH and anSAH, focusing on higher-order

prefrontal functions. Subsequently, we present a study on a broad range of

aspects of social cognition after aSAH in chapter 5. In this chapter, relationships

between behavioral disturbances and focal as well as diffuse brain damage will

also be described. The predictive value of cognitive functions for return to work

is studied in chapter 6. Chapter 7 is a general discussion of the preceding

articles, with final conclusions and implications of our findings.

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